Whole-body endothermy: ancient, homologous and widespread among the ancestors of mammals, birds and crocodylians.

The whole-body (tachymetabolic) endothermy seen in modern birds and mammals is long held to have evolved independently in each group, a reasonable assumption when it was believed that its earliest appearances in birds and mammals arose many millions of years apart. That assumption is consistent with current acceptance that the non-shivering thermogenesis (NST) component of regulatory body heat originates differently in each group: from skeletal muscle in birds and from brown adipose tissue (BAT) in mammals. However, BAT is absent in monotremes, marsupials, and many eutherians, all whole-body endotherms. Indeed, recent research implies that BAT-driven NST originated more recently and that the biochemical processes driving muscle NST in birds, many modern mammals and the ancestors of both may be similar, deriving from controlled 'slippage' of Ca2+ from the sarcoplasmic reticulum Ca2+ -ATPase (SERCA) in skeletal muscle, similar to a process seen in some fishes. This similarity prompted our realisation that the capacity for whole-body endothermy could even have pre-dated the divergence of Amniota into Synapsida and Sauropsida, leading us to hypothesise the homology of whole-body endothermy in birds and mammals, in contrast to the current assumption of their independent (convergent) evolution. To explore the extent of similarity between muscle NST in mammals and birds we undertook a detailed review of these processes and their control in each group. We found considerable but not complete similarity between them: in extant mammals the 'slippage' is controlled by the protein sarcolipin (SLN), in birds the SLN is slightly different structurally and its role in NST is not yet proved. However, considering the multi-millions of years since the separation of synapsids and diapsids, we consider that the similarity between NST production in birds and mammals is consistent with their whole-body endothermy being homologous. If so, we should expect to find evidence for it much earlier and more widespread among extinct amniotes than is currently recognised. Accordingly, we conducted an extensive survey of the palaeontological literature using established proxies. Fossil bone histology reveals evidence of sustained rapid growth rates indicating tachymetabolism. Large body size and erect stature indicate high systemic arterial blood pressures and four-chambered hearts, characteristic of tachymetabolism. Large nutrient foramina in long bones are indicative of high bone perfusion for rapid somatic growth and for repair of microfractures caused by intense locomotion. Obligate bipedality appeared early and only in whole-body endotherms. Isotopic profiles of fossil material indicate endothermic levels of body temperature. These proxies led us to compelling evidence for the widespread occurrence of whole-body endothermy among numerous extinct synapsids and sauropsids, and very early in each clade's family tree. These results are consistent with and support our hypothesis that tachymetabolic endothermy is plesiomorphic in Amniota. A hypothetical structure for the heart of the earliest endothermic amniotes is proposed. We conclude that there is strong evidence for whole-body endothermy being ancient and widespread among amniotes and that the similarity of biochemical processes driving muscle NST in extant birds and mammals strengthens the case for its plesiomorphy.

The ecological importance of crocodylians: towards evidence-based justification for their conservation.

Large-bodied predators are well represented among the world's threatened and endangered species. A significant body of literature shows that in terrestrial and marine ecosystems large predators can play important roles in ecosystem structure and functioning. By contrast, the ecological roles and importance of large predators within freshwater ecosystems are poorly understood, constraining the design and implementation of optimal conservation strategies for freshwater ecosystems. Conservationists and environmentalists frequently promulgate ecological roles that crocodylians are assumed to fulfil, but often with limited evidence supporting those claims. Here, we review the available information on the ecological importance of crocodylians, a widely distributed group of predominantly freshwater-dwelling, large-bodied predators. We synthesise information regarding the role of crocodylians under five criteria within the context of modern ecological concepts: as indicators of ecological health, as ecosystem engineers, apex predators, keystone species, and as contributors to nutrient and energy translocation across ecosystems. Some crocodylians play a role as indicators of ecosystem health, but this is largely untested across the order Crocodylia. By contrast, the role of crocodylian activities in ecosystem engineering is largely anecdotal, and information supporting their assumed role as apex predators is currently limited to only a few species. Whether crocodylians contribute significantly to nutrient and energy translocation through cross-ecosystem movements is unknown. We conclude that most claims regarding the importance of crocodylians as apex predators, keystone species, ecosystem engineers, and as contributors to nutrient and energy translocation across ecosystems are mostly unsubstantiated speculation, drawn from anecdotal observations made during research carried out primarily for other purposes. There is a paucity of biological research targeted directly at: understanding population dynamics; trophic interactions within their ecological communities; and quantifying the short- and long-term ecological impacts of crocodylian population declines, extirpations, and recoveries. Conservation practices ideally need evidence-based planning, decision making and justification. Addressing the knowledge gaps identified here will be important for achieving effective conservation of crocodylians.

Strategic (adaptive) hypothermia in bull dromedary camels during rut; could it increase reproductive success?

In this study of body temperatures (T(b)) in free ranging dromedary camels, we found that bulls in rut start the days cooler. Daily minima during rut averaged 0.6 degrees C lower than at other times (95% CI 0.27-0.94 degrees C) and daily maxima averaged 0.45 degrees C higher (95% CI -0.01 to -0.91 degrees C), increasing the daily T(b) cycle. Knut Schmidt-Nielsen described a similar pattern in captive dromedaries deprived of water in hot conditions, which he interpreted as a strategy to conserve water. Our observations were made in winter and with water freely available. Dromedaries can apparently employ heterothermy for more than just water conservation. In the strenuous daily contests between rival bulls in rut, a lower T(b) early in the day should extend the time for which a contestant can challenge or defend before heat stress becomes a problem. Calculations show that lowering T(b) by even 0.6 degrees C extends that time by more than 30 min, and many daily minima during rut were lower than that. Because the eventual winner of contests gains or retains a herd of females, we speculate that cooler T(b) at the start of daily contests confers an advantage which translates directly into increased reproductive success.

The exceptional longevity of an egg-laying mammal, the short-beaked echidna (Tachyglossus aculeatus) is associated with peroxidation-resistant membrane composition.

The echidna Tachyglossus aculeatus is a monotreme mammal from Australia that is exceptionally long-living. Its documented maximum lifespan of 50 years is 3.7 times that predicted from its body mass. Other exceptionally long-living mammals (naked mole-rats and humans) are known to have peroxidation-resistant membrane composition, raising the question about echidnas. Phospholipids were extracted from skeletal muscle, liver and liver mitochondria of echidnas and fatty acid composition measured. As with other exceptionally long-living mammals, membrane lipids of echidna tissues were found to have a lower content of polyunsaturates and a higher content of monounsaturates than predicted for their body size. The peroxidation index (=peroxidation susceptibility) calculated from this membrane composition was lower-than-expected for their body size, indicating that the cellular membranes of echidnas would be peroxidation-resistant. Additionally when the calculated peroxidation index was plotted against maximum lifespan, the echidna values conformed to the relationship for mammals in general. These findings support the membrane pacemaker theory of aging and emphasise the potential importance of membrane fatty acid composition in aging and in the determination of maximum longevity.

Satellite tracking reveals long distance coastal travel and homing by translocated estuarine crocodiles, Crocodylus porosus.

Crocodilians have a wide distribution, often in remote areas, are cryptic, secretive and are easily disturbed by human presence. Their capacity for large scale movements is poorly known. Here, we report the first study of post-release movement patterns in translocated adult crocodiles, and the first application of satellite telemetry to a crocodilian. Three large male Crocodylus porosus (3.1-4.5 m) were captured in northern Australia and translocated by helicopter for 56, 99 and 411 km of coastline, the last across Cape York Peninsula from the west coast to the east coast. All crocodiles spent time around their release site before returning rapidly and apparently purposefully to their capture locations. The animal that circumnavigated Cape York Peninsula to return to its capture site, travelled more than 400 km in 20 days, which is the longest homeward travel yet reported for a crocodilian. Such impressive homing ability is significant because translocation has sometimes been used to manage potentially dangerous C. porosus close to human settlement. It is clear that large male estuarine crocodiles can exhibit strong site fidelity, have remarkable navigational skills, and may move long distances following a coastline. These long journeys included impressive daily movements of 10-30 km, often consecutively.

Respiratory properties of blood in flatback turtles (Natator depressus).

Oxygen equilibrium curves and other respiratory-related variables were determined on blood from the flatback turtle (Natator depressus) and, for comparison, on some samples from the loggerhead turtle (Caretta caretta). The oxygen carrying capacity of the flatback turtle, 4.9-8.7 mmol l(-1) (n = 49), is at the high end of the range in diving reptiles. Oxygen affinity (P(50)) was similar in both species at 5% CO(2), ranging from 37 to 55 mmHg (43 mmHg +/- 5.3 SD, n = 24, 25 degrees C, pH 7.17) in flatbacks and 43-49 mmHg in loggerheads (46 mmHg +/- 2.0 SD, n = 7, 25 degrees C, pH 7.13), whereas at 2% CO(2), flatbacks had a higher oxygen affinity. The curves differed in sigmoidicity, with Hill n coefficients of 2.8 and 1.9 in flatbacks and loggerheads, respectively. The Bohr effect was small in both the species, consistent with results from other sea turtles. Lactate levels were high, perhaps because the samples were taken from turtles coming ashore to lay eggs. Flatbacks are rarely found in waters deeper than 45 m. It is suggested that they have a respiratory physiology particularly suited to sustain prolonged shallow dives.

Respiration by buried echidnas Tachyglossus aculeatus.

Short-beaked echidnas have an impressive ability to submerge completely into soil or sand and remain there, cryptic, for long periods. This poses questions about how they manage their respiration, cut off from a free flow of gases. We measured the gradient in oxygen partial pressure (PO2) away from the snouts of buried echidnas and oxygen consumption (VO2) in five individuals under similar conditions, in two substrates with different air-filled porosities (fa). A theoretical diffusion model indicated that diffusion alone was insufficient to account for the flux of oxygen required to meet measured rates of VO2. However, it was noticed that echidnas often showed periodic movements of the anterior part of the body, as if such movements were a deliberate effort to flush the tidal air space surrounding their nostrils. These ;flushing movements' were subsequently found to temporarily increase the levels of interstitial oxygen in the soil around the head region. Flushing movements were more frequent while VO2 was higher during the burrowing process, and also in substrate with lower fa. We conclude that oxygen supply to buried echidnas is maintained by diffusion through the soil augmented by periodic flushing movements, which ventilate the tidal airspace that surrounds the nostrils.

Temperature and the respiratory properties of whole blood in two reptiles, Pogona barbata and Emydura signata.

We investigated the capacity of two reptiles, an agamid lizard Pogona barbata and a chelid turtle Emydura signata, to compensate for the effects of temperature by making changes in their whole blood respiratory properties. This was accomplished by measuring the P50 (at 10, 20 and 30 degrees C), hematocrit (Hct), haemoglobin concentration ([Hb]) and mean cell haemoglobin concentration (MCHC) in field acclimatised and laboratory acclimated individuals. The acute effect of temperature on P50 in P. barbata, expressed as heat of oxygenation (deltaH), ranged from -16.8+/-1.84 to -28.5+/-2.73 kJ/mole. P50 of field acclimatised P. barbata increased significantly from early spring to summer at the test temperatures of 20 degrees C (43.1+/-1.2 to 48.8+/-2.1 mmHg) and 30 degrees C (54.7+/-1.2 to 65.2+/-2.3 mmHg), but showed no acclimation under laboratory conditions. For E. signata, deltaH ranged from -31.1+/-6.32 to -48.2+/-3.59 kJ/mole. Field acclimatisation and laboratory acclimation of P50 did not occur. However, in E. signata, there was a significant increase in [Hb] and MCHC from early spring to summer in turtles collected from the wild (1.0+/-0.1 to 1.7+/-0.2 mmol/L and 4.0+/-0.3 to 6.7+/-0.7 mmol/L, respectively).

The evolution of endothermy and its diversity in mammals and birds.

Many elements of mammalian and avian thermoregulatory mechanisms are present in reptiles, and the changes involved in the transition to endothermy are more quantitative than qualitative. Drawing on our experience with reptiles and echidnas, we comment on that transition and on current theories about how it occurred. The theories divide into two categories, depending on whether selection pressures operated directly or indirectly on mechanisms producing heat. Both categories of theories focus on explaining the evolution of homeothermic endothermy but ignore heterothermy. However, noting that hibernation and torpor are almost certainly plesiomorphic (=ancestral, primitive), and that heterothermy is very common among endotherms, we propose that homeothermic endothermy evolved via heterothermy, with the earliest protoendotherms being facultatively endothermic and retaining their ectothermic capacity for "constitutional eurythermy." Thus, unlike current models for the evolution of endothermy that assume that hibernation and torpor are specialisations arising from homeothermic ancestry, and therefore irrelevant, we consider that they are central. We note the sophistication of thermoregulatory behavior and control in reptiles, including precise control over conductance, and argue that brooding endothermy seen in some otherwise ectothermic Boidae suggests an incipient capacity for facultative endothermy in reptiles. We suggest that the earliest insulation in protoendotherms may have been internal, arising from redistribution of the fat bodies that are typical of reptiles. We note that short-beaked echidnas provide a useful living model of what an (advanced) protoendotherm may have been like. Echidnas have the advantages of endothermy, including the capacity for homeothermic endothermy during incubation, but are very relaxed in their thermoregulatory precision and minimise energetic costs by using ectothermy facultatively when entering short- or long-term torpor. They also have a substantial layer of internal dorsal insulation. We favor theories about the evolution of endothermy that invoke direct selection for the benefits conferred by warmth, such as expanding daily activity into the night, higher capacities for sustained activity, higher digestion rates, climatic range expansion, and, not unrelated, control over incubation temperature and the benefits for parental care. We present an indicative, stepwise schema in which observed patterns of body temperature are a consequence of selection pressures, the underlying mechanisms, and energy optimization, and in which homeothermy results when it is energetically desirable rather than as the logical endpoint.

Evidence for endothermic ancestors of crocodiles at the stem of archosaur evolution.

Physiological, anatomical, and developmental features of the crocodilian heart support the paleontological evidence that the ancestors of living crocodilians were active and endothermic, but the lineage reverted to ectothermy when it invaded the aquatic, ambush predator niche. In endotherms, there is a functional nexus between high metabolic rates, high blood flow rates, and complete separation of high systemic blood pressure from low pulmonary blood pressure in a four-chambered heart. Ectotherms generally lack all of these characteristics, but crocodilians retain a four-chambered heart. However, crocodilians have a neurally controlled, pulmonary bypass shunt that is functional in diving. Shunting occurs outside of the heart and involves the left aortic arch that originates from the right ventricle, the foramen of Panizza between the left and right aortic arches, and the cog-tooth valve at the base of the pulmonary artery. Developmental studies show that all of these uniquely crocodilian features are secondarily derived, indicating a shift from the complete separation of blood flow of endotherms to the controlled shunting of ectotherms. We present other evidence for endothermy in stem archosaurs and suggest that some dinosaurs may have inherited the trait.

Body temperature in captive long-beaked echidnas (Zaglossus bartoni).

The routine occurrence of both short-term (daily) and long-term torpor (hibernation) in short-beaked echidnas, but not platypus, raises questions about the third monotreme genus, New Guinea's Zaglossus. We measured body temperatures (T(b)) with implanted data loggers over three and a half years in two captive Zaglossus bartoni at Taronga Zoo, Sydney. The modal T(b) of both long-beaks was 31 degrees C, similar to non-hibernating short-beaked echidnas, Tachyglossus aculeatus, in the wild (30-32 degrees C) and to platypus (32 degrees C), suggesting that this is characteristic of normothermic monotremes. T(b) cycled daily, usually over 2-4 degrees C. There were some departures from this pattern to suggest periods of inactivity but nothing to indicate the occurrence of long-term torpor. In contrast, two short-beaked echidnas monitored concurrently in the same pen showed extended periods of low T(b) in the cooler months (hibernation) and short periods of torpor at any time of the year, as they do in the wild. Whether torpor or hibernation occurs in Zaglossus in the wild or in juveniles remains unknown. However, given that the environment in this study was conducive to hibernation in short-beaks, which do not easily enter torpor in captivity, and their large size, we think that torpor in wild adult Zaglossus is unlikely.

Physiological responses to prolonged aquatic hypoxia in the Queensland lungfish Neoceratodus forsteri.

The effects of moderate and severe hypoxia on air breathing frequency and respiratory properties of the blood of the Queensland (Australian) lungfish Neoceratodus forsteri were measured in fish exposed to these conditions for 14-22 days at 20 degrees C. Haemoglobin oxygen affinity increased after exposure to moderate hypoxia (PW(O(2)) = 60 mmHg), but did not increase further after exposure to severe hypoxia (PW(O(2)) = 40 mmHg). The P(50) of whole blood (20 degrees C, P(CO(2)) = 16.0 mmHg) fell from 22.0 +/- 1.5 mmHg in normoxic conditions to 19.0 +/- 1.0 mmHg in hypoxic conditions. Under both moderate and severe hypoxia, haematocrit, haemoglobin, blood lactate, and erythrocyte phosphate concentrations did not differ from normoxic values. The observed increase in haemoglobin oxygen affinity in response to aquatic hypoxia is typical of compensatory responses seen in obligate water breathers, but smaller. This suggests that the capacity of lungfish to respond to hypoxia by breathing air removes the necessity for further left-shifting of the oxygen equilibrium curve.

Thermal ecology of the Australian agamid Pogona barbata.

This study compares the thermal ecology of male bearded dragon lizards (Pogona barbata) from south-east Queensland across two seasons: summer (1994-1995) and autumn (1995). Seasonal patterns of body temperature (T b) were explored in terms of changes in the physical properties of the thermal environment and thermoregulatory effort. To quantify thermoregulatory effort, we compared behavioral and physiological variables recorded for observed lizards with those estimated for a thermoconforming lizard. The study lizards' field T bs varied seasonally (summer: grand daily mean (GDM) 34.6 ± 0.6°C, autumn: GDM 27.5 ± 0.3°C) as did maximum and minimum available operative temperatures (summer: GDM T max 42.1 ± 1.7°C, T min 32.2 ± 1.0°C, autumn: GDM T max 31.7 ± 1.2°C, T min 26.4 ± 0.5°C). Interestingly, the range of temperatures that lizards selected in a gradient (selected range) did not change seasonally. However, P. barbata thermoregulated more extensively and more accurately in summer than in autumn; lizards generally displayed behaviors affecting heat load nonrandomly in summer and randomly in autumn, leading to the GDM of the mean deviations of lizards' field T bs from their selected ranges being only 2.1 ± 0.5°C in summer, compared to 4.4 ± 0.5°C in autumn. This seasonal difference was not a consequence of different heat availability in the two seasons, because the seasonally available ranges of operative temperatures rarely precluded lizards from attaining field T bs within their selected range, should that have been the goal. Rather, thermal microhabitat distribution and social behavior appear to have had an important influence on seasonal levels of thermoregulatory effort.

Increased vascularity of the lingual salt glands of the estuarine crocodile, Crocodylus porosus, kept in hyperosmotic salinity.

Methyl methacrylate corrosion casts were made of the blood-vascular system of the lingual salt glands of the estuarine crocodile, Crocodylus porosus, and examined with light and scanning electron microscopy. The 28-40 individual salt glands, each opening separately via a single pore onto the dorsal surface of the tongue, are supplied by a pair of lingual arteries. Each gland is richly vascularized and is composed of 14-20 lobular sub-units, each having a dense network of capillaries. The blood flow in each gland is from the centre to its periphery, opposite to the direction of the flow of secretions in the ducts of the gland. The main collecting duct leading from the gland to the external pore was well vascularized. The blood supply to the glands of juvenile crocodiles raised in 20‰ salt water was more dense than in freshwater and, from cast masses, had a three-fold greater vascular volume. This study provides the first evidence which shows that the salt glands of crocodiles are morphologically labile and can adapt to the environmental salinity. © 1993 Wiley-Liss, Inc.

Validation and use of 22Na turnover to measure food intake in free-ranging lizards.

As the food intake of free-ranging animals has proved to be difficult to measure by traditional means, the feasibility of using radioactive Na to measure food consumption in a small scincid lizard (Lampropholis guichenoti) was assessed. This technique has previously been used only for several species of mammal. A significant relationship between food intake and Na turnover was found in the laboratory, with Na turnover underestimating intake by 7.6%. The food intake of free-ranging members of a field population was estimated by 22Na turnover to be 9.55, 0.65, 9.39 and 13.75 mg dry weight (day)-1 during autumn, winter, spring and summer respectively. Estimates of assimilated and expended energy from these food intake values agree closely with data reported for other lizards using alternative techniques. This study also describes the technical innovations which were necessary to study lizards weighing less than 1 g; and it suggests that 22Na can provide an easy, reliable and inexpensive means of studying the energetics of many free-living animals.